Gabrielle A. Nevitt

Olfactory Foraging by Antarctic Procellariiform Seabirds: Life at High Reynolds Numbers

Antarctic procellariiform seabirds forage over vast stretches of open ocean in search of patchily distributed prey resources. These seabirds are unique in that most species have anatomically well-developed olfactory systems and are thought to have an excellent sense of smell. Results from controlled experiments performed at sea near South Georgia Island in the South Atlantic indicate that different species of procellariiforms are sensitive to a variety of scented compounds associated with their primary prey. These include krill-related odors (pyrazines and trimethylamine) as well as odors more closely associated with phytoplankton (dimethyl sulfide, DMS). Data collected in the context of global climatic regulation suggest that at least one of these odors (DMS) tends to be associated with predictable bathymetry, including upwelling zones and seamounts. Such odor features are not ephemeral but can be present for days or weeks. I suggest that procellariiforms foraging over vast distances may be able to recognize these features reflected in the olfactory landscape over the ocean. On the large scale, such features may aid seabirds in navigation or in locating profitable foraging grounds. Once in a profitable foraging area, procellariiforms may use olfactory cues on a small scale to assist them in locating prey patches.

Early rearing environment impacts cerebellar growth in juvenile salmon

SUMMARY The size and structure of an animals brain is typically assumed to result from either natural or artificial selection pressures over generations. However, because a fishs brain grows continuously throughout life, it may be particularly responsive to the environmental conditions the fish experiences during development. Salmon are an ideal model system for studying these effects because natural habitats differ significantly from the hatchery environments in which these fish are frequently reared. For example, in the wild, salmon alevins (i.e. yolk-sac fry) are buried in the gravel, while hatchery environments lack this structural component. We show that the simple manipulation of adding stones to a standard rearing tank can dramatically alter the growth of specific brain structures in steelhead salmon alevins (Oncorhynchus mykiss). We found that alevins reared with stones grew brains with significantly larger cerebella than genetically similar fish reared in conventional tanks. This shift to a larger cerebellar size was, in turn, accompanied by changes in locomotory behaviors - behaviors that correlate strongly to the function of this brain region. We next show that hatchery fish reared in a more naturalistic setting in the wild had significantly larger brains than their lab-reared counterparts. However, relative cerebellar volumes were similar between wild-reared alevins and those reared in the complex treatment in the laboratory. Together our results indicate that, within the first three weeks of life, variation in rearing environment can result in brain differences that are commonly attributed to generations of selection. These results highlight the need to consider enrichment strategies when designing captive rearing facilities for both conservation and laboratory use.

Sensory ecology on the high seas: the odor world of the procellariiform seabirds

SUMMARY Procellariiform seabirds wander the worlds oceans aided by olfactory abilities rivaling those of any animal on earth. Over the past 15 years, I have been privileged to study the sensory ecology of procellariiforms, focusing on how olfaction contributes to behaviors, ranging from foraging and navigation to individual odor recognition, in a broader sensory context. We have developed a number of field techniques for measuring both olfactory- and visually based behaviors in chicks and adults of various species. Our choice of test odors has been informed by long-term dietary studies and geochemical data on the production and distribution of identifiable, scented compounds found in productive waters. This multidisciplinary approach has shown us that odors provide different information over the ocean depending on the spatial scale. At large spatial scales (thousands of square kilometers), an olfactory landscape superimposed upon the ocean surface reflects oceanographic or bathymetric features where phytoplankton accumulate and an area-restricted search for prey is likely to be successful. At small spatial scales (tens to hundreds of square kilometers), birds use odors and visual cues to pinpoint and capture prey directly. We have further identified species-specific, sensory-based foraging strategies, which we have begun to explore in evolutionary and developmental contexts. With respect to chemical communication among individuals, we have shown that some species can distinguish familiar individuals by scent cues alone. We are now set to explore the mechanistic basis for these discriminatory abilities in the context of kin recognition, and whether or not the major histocompatibility complex is involved.

Evidence for olfactory search in wandering albatross, Diomedea exulans

Wandering albatrosses (Diomedea exulans) forage over thousands of square kilometers of open ocean for patchily distributed live prey and carrion. These birds have large olfactory bulbs and respond to fishy-scented odors in at-sea trials, suggesting that olfaction plays a role in natural foraging behavior. With the advent of new, fine-scale tracking technologies, we are beginning to explore how birds track prey in the pelagic environment, and we relate these observations to models of odor transport in natural situations. These models suggest that odors emanating from prey will tend to disperse laterally and downwind of the odor source and acquire an irregular and patchy concentration distribution due to turbulent transport. For a seabird foraging over the ocean, this scenario suggests that olfactory search would be facilitated by crosswind flight to optimize the probability of encountering a plume emanating from a prey item, followed by upwind, zigzag flight to localize the prey. By contrast, birds approaching prey by sight would be expected to fly directly to a prey item, irrespective of wind direction. Using high-precision global positioning system (GPS) loggers in conjunction with stomach temperature recorders to simultaneously monitor feeding events, we confirm these predictions in freely ranging wandering albatrosses. We found that initial olfactory detection was implicated in nearly half (46.8%) of all flown approaches preceding prey-capture events, accounting for 45.5% of total prey mass captured by in-flight foraging. These results offer insights into the sensory basis for area-restricted search at the large spatial scales of the open ocean.

Effects of Hatchery Rearing on Brain Structures of Rainbow Trout, Oncorhynchus mykiss

In this study, we contrast brain morphology from hatchery and wild reared stocks to examine the hypothesis that in salmonid fishes, captive rearing produces changes in brain development. Using rainbow trout, Oncorhynchus mykiss, as a model, we measured eight regions of the salmonid brain to examine differences between wild and hatchery reared fish. We find using multiple analysis of covariance (MANCOVA), analysis of covariance (ANCOVA) and discriminant function analysis (DFA) that the brains of hatchery reared fish are relatively smaller in several critical measures than their wild counterparts. Our work may suggest a mechanistic basis for the observed vulnerability of hatchery fish to predation and their general low survival upon release into the wild. Our results are the first to highlight the effects of hatchery rearing on changes in brain development inbreak fishes.

Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds

Petrels, albatrosses and other procellariiform seabirds have an excellent sense of smell, and routinely navigate over the worlds oceans by mechanisms that are not well understood. These birds travel thousands of kilometres to forage on ephemeral prey patches at variable locations, yet they can quickly and efficiently find their way back to their nests on remote islands to provision chicks, even with magnetic senses experimentally disrupted. Over the seemingly featureless ocean environment, local emissions of scents released by phytoplankton reflect bathymetric features such as shelf breaks and seamounts. These features suggest an odour landscape that may provide birds with orientation cues. We have previously shown that concentrated experimental deployments of one such compound, dimethyl sulphide (DMS), attracts procellariiforms at sea, suggesting that some species can use it as a foraging cue. Here we present the first physiological demonstration that an Antarctic seabird can detect DMS at biogenic levels. We further show that birds can use DMS as an orientation cue in a non-foraging context within a concentration range that they might naturally encounter over the ocean.

Evidence that thyroid hormone induces olfactory cellular proliferation in salmon during a sensitive period for imprinting

SUMMARY Salmon have long been known to imprint and home to natal stream odors, yet the mechanisms driving olfactory imprinting remain obscure. The timing of imprinting is associated with elevations in plasma thyroid hormone levels, with possible effects on growth and proliferation of the peripheral olfactory system. Here, we begin to test this idea by determining whether experimentally elevated plasma levels of 3,5,3′-triiodothyronine (T3) influence cell proliferation as detected by the 5-bromo-2′-deoxyuridine (BrdU) cell birth-dating technique in the olfactory epithelium of juvenile coho salmon (Oncorhynchus kisutch). We also explore how natural fluctuations in thyroxine (T4) relate to proliferation in the epithelium during the parr-smolt transformation. In both studies, we found that BrdU labeled both single and clusters of mitotic cells. The total number of BrdU-labeled cells in the olfactory epithelium was significantly greater in fish with artificially elevated T3 compared with placebo controls. This difference in proliferation was restricted to the basal region of the olfactory epithelium, where multipotent progenitor cells differentiate into olfactory receptor neurons. The distributions of mitotic cluster sizes differed significantly from a Poisson distribution for both T3 and placebo treatments, suggesting that proliferation tends to be non-random. Over the course of the parr-smolt transformation, changes in the density of BrdU cells showed a positive relationship with natural fluctuations in plasma T4. This relationship suggests that even small changes in thyroid activity can stimulate the proliferation of neural progenitor cells in the salmon epithelium. Taken together, our results establish a link between the thyroid hormone axis and measurable anatomical changes in the peripheral olfactory system.

Exogenous vasotocin alters aggression during agonistic exchanges in male Amargosa River pupfish (Cyprinodon nevadensis amargosae)

Pupfishes in the Death Valley region have rapidly differentiated in social behaviors since their isolation in a series of desert streams, springs, and marshes less than 20,000 years ago. These habitats can show dramatic fluctuations in ecological conditions, and pupfish must cope with the changes by plastic physiological and behavioral responses. Recently, we showed differences among some Death Valley populations in brain expression of arginine vasotocin (AVT). As AVT regulates both hydromineral balance and social behaviors in other taxa, these population differences may indicate adaptive changes in osmoregulatory and/or behavioral processes. To test whether AVT is relevant for behavioral shifts in these fish, here we examined how manipulations to the AVT system affect agonistic and reproductive behaviors in Amargosa River pupfish (Cyprinodon nevadensis amargosae). We administered exogenous AVT (0.1, 1, and 10 microg/g body weight) and an AVP V1 receptor antagonist (Manning compound, 2.5 microg/g body weight) intraperitoneally to males in mixed-sex groups in the laboratory. We found that AVT reduced the initiation of aggressive social interactions with other pupfish but had no effect on courtship. The effects of AVT were confirmed in males in the wild where AVT (1 microg/g body weight) reduced the aggressive initiation of social interactions and decreased aggressive responses to the behavior of other males. Combined, these results show that AVT can modulate agonistic behaviors in male pupfish and support the idea that variation in AVT activity may underlie differences in aggression among Death Valley populations.

The use of odors at different spatial scales: comparing birds with fish.

Salmon travel hundreds of kilometers of open ocean and meandering rivers to return to their natal stream to spawn; procellariiform seabirds soar over thousands of kilometers of the ocean’s surface searching for foraging opportunities and accurately return to their nesting islands. These large-scale olfactory-guided behaviors are among the most dramatic examples of animal navigation ever described. At much closer ranges, the sense of smell can be used for behaviors as diverse as tracking prey, nest location, and mate selection. Both fish and birds face similar problems interpreting olfactory information in fluid mediums where odors are dispersed as filamentous patches. Similar to insects, which have served as model organisms for investigating olfactory related behaviors, the few fish and bird species that have been studied tend to use olfactory information in conjunction with other sensory modalities. Similar to insects, fish and birds also employ oscillatory or cross-stream movement as sampling mechanisms. This review compares and contrasts the use of odors by fish and birds over a range of spatial scales that span from thousands of kilometers to less than a meter. In so doing, we identify behavioral similarities and new questions that need to be addressed regarding the olfactory ecology of these diverse groups of organisms.

Evidence for nest-odour recognition in two species of diving petrel.

SUMMARY In nearly every procellariiform species, the sense of smell appears to be highly adapted for foraging at sea, but the sense of smell among the diving petrels is enigmatic. These birds forage at considerable depth and are not attracted to odour cues at sea. However, several procellariiform species have recently been shown to relocate their nesting burrows by scent, suggesting that these birds use an olfactory signature to identify the home burrow. We wanted to know whether diving petrels use smell in this way. We tested the common diving petrel Pelecanoides urinatrix and the South-Georgian diving petrel Pelecanoides georgicus to determine whether diving petrels were able to recognise their burrow by scent alone. To verify the efficacy of the method, we also tested a bird that is known to use olfaction for foraging and nest recognition, the thin-billed prion Pachyptila belcheri. In two-choice T-maze trials, we found that, for all species, individuals significantly preferred the odour of their own nest material to that of a conspecific. Our findings strongly suggest that an individual-specific odour provides an olfactory signature that allows burrowing petrels to recognize their own burrow. Since this ability seems to be well developed in diving petrels, our data further implicate a novel adaptation for olfaction in these two species that have been presumed to lack a well-developed sense of smell.